OpEd: The Repeater.

January 29, 2008, 6:52 pm
http://judson.blogs.nytimes.com/2008/01/29/the-repeater/?ref=opinion

The Repeater

Here?s an evolutionist?s dream: 10,000 planet Earths, starting from
the same point at the same time, and left to their own devices for
four and a half billion years. What would happen? Could you go on
safari from one planet to the next seeing an endless procession of
wildly different organisms? Or would many of the planets be home to
life forms that are broadly similar?

The conventional answer to this question ? the one championed by the
late Stephen Jay Gould, for example ? is that chance events, from
mutations to asteroids, play such a large role in evolution that each
of the planets would be totally different. And probably, after four
and a half billion years, they would be. I wish we could do the
experiment, though. It might hold some surprises.

Looking around the Earth, it?s striking how often similar traits
evolve in similar environments. So: birds living on remote islands
typically lose the power of flight. Males in species (be they
chimpanzees or yellow dung flies) where females are promiscuous tend
to evolve high sperm counts and large testes. Animals that live in
caves lose their eyes and their color: whether they live in Rwanda or
Romania, they?re a pallid, blind lot, the troglodytes. Mammals that
specialize on eating leaves ? be they cows or langurs (that?s a
monkey) ? have evolved foreguts where bacteria break down the leaves,
as well as special enzymes to help with digestion. Amazingly, the same
phenomena are also seen in the hoatzin, a leaf-eating bird from South
America. In short, evolution has a remarkable tendency to repeat
itself.

That this happens has been known for decades. But now we?re unpicking
the genetic basis for the repetitions. And the startling thing is,
evolution often repeats itself at the genetic level, too.

As an example, take three-spine sticklebacks (Gasterosteus aculeatus).
These little fish usually live in the ocean, but like salmon, they
come into rivers to spawn. As the glaciers retreated at the end of the
last ice age ? a process that went on between ten and twenty thousand
years ago ? a series of lakes began to form in the northern
hemisphere, and the sticklebacks moved into them. Initially, the lakes
would have been linked to the oceans by streams and rivers, but as the
glaciers retreated, the land rose up (ice is heavy), and the exits to
the lakes closed, leaving the sticklebacks in each lake marooned and
isolated. And so the animals stuck there began evolving to live
exclusively in freshwater.

Which is a real-life version of the evolutionist?s dream: each lake is
an evolutionary experiment, a natural laboratory. Because there are so
many lakes, the experiment has been repeated many times; and because
we know the ages of the lakes, we know roughly how long each
experiment has been going on. And sure enough, fish in different lakes
have evolved a variety of similar features, repeatedly and
independently.

Marine sticklebacks, for example, boast body armor: from head to tail,
they are covered in rows of bony plates. Many freshwater sticklebacks
have lost these. In marine sticklebacks, the pelvis is a complicated
affair that comes complete with a pair of long spines. In some
freshwater populations, individuals have a much reduced, lopsided
pelvic structure. In others, they have just a remnant, a small,
lopsided bone: the ghost of pelvis past.

Mutations to a gene called Ectodysplasin have been implicated as the
major culprit in loss of armor; another gene, Pitx1, has been fingered
as the main agent of pelvis reduction. Yet the means by which the two
genes have effected their changes are different.

Take Ectodysplasin first. In this case, a rare version of the gene
exists at a low frequency in marine sticklebacks. Two copies of the
rare version (you inherit one from each of your parents), and you have
no plates. Two copies of the regular version, and you have all the
plates. But if you have one of each, the sort of armor you have can
vary. Some individuals will have all their plates. Others will have a
sort of half-armor.

What seems to have happened is that when sticklebacks invaded each
lake, some of the invaders carried this rare version with them. In the
ocean, being without body armor is deadly: it makes you vulnerable to
predators. But lakes don?t have the same dangers as the ocean ? and
armor is heavy and makes you less agile. Thus, in these new
environments, being without body armor conferred a significant
advantage, and so in lake after lake, the rare variant of the gene
swept through the population.

Let?s turn now to the ghostly pelvis. Pelvic loss is much less common
than armor loss. But if you find sticklebacks that lack a pelvis, you
can bet that they came from large, shallow lakes where the water is
soft, there are no large fish that might act as predators, and the
vegetation is dense. Soft water has little calcium, and you need
calcium to make the pelvic spines. Shallow lakes that are thick with
weeds are home to predators like dragonflies, which enjoy having a
stickleback for breakfast. And whereas the spines are a defense
against being eaten by other fish ? trout, say, or pike ? and can
actually induce the predator to spit out the stickleback instead of
trying to swallow it, insect predators catch sticklebacks by grabbing
the spines.

The difference between having a spiky pelvis or not is influenced by
the expression of several genes, but as I said earlier, the main agent
seems to be a gene called Pitx1. In sticklebacks with a proper pelvis,
this gene is turned on at several different places in the developing
fish, including the head, the pituitary and the spots on the side of
the body where the pelvis should form. In those without, Pitx1 is
switched on everywhere except the pelvic region, and the pelvis
doesn?t grow.

There are a couple of interesting things about this discovery. The
first is that the molecular basis of the change from pelvis to no
pelvis does not involve a mutation to the protein-coding region of the
Pitx1 gene itself. In other words, the protein made from the gene
hasn?t changed. What has changed is the way the gene is expressed.
This is in contrast to the sorts of mutations one often reads about as
being involved in evolution, which typically involve changes to the
protein itself.

A second interesting feature of the stickleback pelvis is that ?
unlike the armor plates ? the loss is probably due to mutations having
occurred independently in the different populations. What?s more,
changes to the use of Pitx1 are also implicated in pelvic loss in
nine-spine sticklebacks (Pungitius pungitius) ? yet nine-spine and
three-spine sticklebacks have been going their own evolutionary ways
for at least 10 million years. Mice that have been genetically
engineered to lack Pitx1 have a suite of abnormalities, including
crushed faces and abnormal pituitaries, that cause them to die young.
Intriguingly, they also have a reduced pelvis and hind limbs, and as
with the sticklebacks, the reduction is lopsided and shows a greater
loss on the right than on the left.

Which makes you wonder. Manatees ? those charming marine mammals that
cavort in the Florida keys and the West Indies ? have also lost their
hind legs. All that?s left of their pelvis is a lopsided bone, smaller
on the right than on the left. Could Pitx1 have been involved here,
too? So far, no one knows for sure. But I?d put money on it.

The idea that the same gene could be involved in mediating evolution
of the same trait in creatures as distantly related as mammals and
fish is exciting. And ? to give one last example ? while the relation
between Pitx1 and the manatee?s missing hind legs is speculative
rather than proven, there is much stronger evidence that a gene called
Kit ligand is involved in mediating the evolution of light skin color
in both sticklebacks and people.

This gene is by no means the only one that affects human skin color;
nonetheless, genetic differences in the regulatory regions of this
gene have a significant effect on how light or dark your skin will be,
or whether you have blond hair. In sticklebacks, meanwhile, pale skin
often evolves in freshwater ? perhaps as a disguise ? and the change
again maps to Kit ligand, and involves alterations in the way Kit
ligand is expressed in particular tissues.

Here, I?ve focused on one particular version of the evolutionist?s
dream. But there are many others. In northeastern Mexico, for
instance, a small fish known as Astyanax has, on a number of
occasions, taken up residence in caves: populations of the fish have
been found in more than 25 caves, some of them hundreds of miles
apart. This system, too, is giving us a glimpse of the genetics of
repeated evolution.

And I haven?t even mentioned the hundreds of actual experiments ?
bacteria or yeasts evolving for generations in the laboratory. Yet all
these systems show the same thing: at the genetic level, evolution is,
to a remarkable extent, a repeater.

**********

NOTES:

Gould discussed the role of contingency in evolution in a number of
books and articles, but see especially Gould, S. J. 2000. ?Wonderful
Life.? Vintage.

Examples of similar traits appearing in similar environments are
numerous, and can be found in any textbook on evolution; but for
details of the hoatzin, see Kornegay, J. R., Schilling, J. W., and
Wilson, A. C.. 1994. ?Molecular adaptation of a leaf-eating bird:
stomach lysozyme of the hoatzin.? Molecular Biology and Evolution 11:
921-928.

For an excellent overview of evolution repeating itself at the genetic
level, see Wood, T. E., Burke, J. M., and Rieseberg, L. H. 2005.
?Parallel genotypic adaptation: when evolution repeats itself.?
Genetica 123: 157-170.

For the genetics of armor inheritance, see Colosimo, P. F., Peichel,
C. L., Nereng, K., Blackman, B. K., Shapiro, M. D., Schluter, D., and
Kingsley, D. M. 2004. ?The genetic architecture of parallel armor
plate reduction in threespine sticklebacks.? PloS Biology 2: 635-641.
For selective sweeps on Ectodysplasin, see Colosimo, P. F., Hosemann,
K. E., Balabhadra, S., Villareal Jr, G., Dickson, M., Grimwood, J.,
Schmutz, J., Myers, R. M., Schluter, D., Kingsley, D. M. 2005.
?Widespread parallel evolution in sticklebacks by repeated fixation of
Ectodysplasin alleles.? Science 307: 1928-1933.

The forces that lead to loss of the pelvis in sticklebacks were
described to me by Dr David Kingsley, of Stanford University, in a
telephone conversation. For the role of Pitx1 in pelvic loss, see
Shapiro, M. D., Marks, M. E., Peichel, C. L., Blackman, B. K., Nereng,
K. S., Jonsson, B., Schulter, D., and Kingsley, D. M. 2004. ?Genetic
and developmental basis of evolutionary pelvic reduction in threespine
sticklebacks.? Nature 428: 717-723. For the comparison between
three-spine and nine-spine sticklebacks and the manatee, see Shapiro,
J. D., Bell, M. A., and Kingsley, D. M. 2006. ?Parallel genetic
origins of pelvic reduction in vertebrates.? Proceedings of the
National Academy of Sciences 103: 13753-13758.

For the evolution of pigmentation in sticklebacks and humans, see
Miller, C. T., Beleza, S., Pollen, A. A., Schluter, D., Kittles, R.
A., Shriver, M. D., and Kingsley, D. M. 2007. ?cis-Regulatory changes
in Kit ligand expression and parallel evolution of pigmentation in
sticklebacks and humans.? Cell 131: 1179-1189.

For more about the Mexican cave fish Astyanax, see Protas, M. E.,
Hersey, C., Kochanek, D., Zhou, Y., Wilkens, H., Jeffery, W. R., Zon,
L. I., Borowsky, R., and Tabin, C. J. 2006. ?Genetic analysis of
cavefish reveals molecular convergence in the evolution of albinism.?
Nature Genetics 38: 107-111.

--
Bob.

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